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Comparative and population genomics of buckwheat species reveal key determinants of flavor and fertility

Comparative and population genomics of buckwheat species reveal key determinants of flavor and fertility
Comparative and population genomics of buckwheat species reveal key determinants of flavor and fertility

Common buckwheat (Fagopyrum esculentum) is an ancient crop with a world-wide distribution. Due to its excellent nutritional quality and high economic and ecological value, common buckwheat is becoming increasingly important throughout the world. The availability of a high-quality reference genome sequence and population genomic data will accelerate the breeding of common buckwheat, but the high heterozygosity due to the outcrossing nature has greatly hindered the genome assembly. Here we report the assembly of a chromosome-scale high-quality reference genome of F. esculentum var. homotropicum, a homozygous self-pollinating variant of common buckwheat. Comparative genomics revealed that two cultivated buckwheat species, common buckwheat (F. esculentum) and Tartary buckwheat (F. tataricum), underwent metabolomic divergence and ecotype differentiation. The expansion of several gene families in common buckwheat, including FhFAR genes, is associated with its wider distribution than Tartary buckwheat. Copy number variation of genes involved in the metabolism of flavonoids is associated with the difference of rutin content between common and Tartary buckwheat. Furthermore, we present a comprehensive atlas of genomic variation based on whole-genome resequencing of 572 accessions of common buckwheat. Population and evolutionary genomics reveal genetic variation associated with environmental adaptability and floral development between Chinese and non-Chinese cultivated groups. Genome-wide association analyses of multi-year agronomic traits with the content of flavonoids revealed that Fh05G014970 is a potential major regulator of flowering period, a key agronomic trait controlling the yield of outcrossing crops, and that Fh06G015130 is a crucial gene underlying flavor-associated flavonoids. Intriguingly, we found that the gene translocation and sequence variation of FhS-ELF3 contribute to the homomorphic self-compatibility of common buckwheat. Collectively, our results elucidate the genetic basis of speciation, ecological adaptation, fertility, and unique flavor of common buckwheat, and provide new resources for future genomics-assisted breeding of this economically important crop.

Fagopyrum, Fertility, Genome-Wide Association Study, Plant Breeding, flavonoids, buckwheat, natural variation, adaptation, genomics
1752-9859
1427-1444
Zhang, Kaixuan
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He, Yuqi
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Lu, Xiang
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Shi, Yaliang
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Zhao, Hui
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Li, Xiaobo
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Li, Jinlong
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Liu, Yang
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Ouyang, Yinan
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Tang, Yu
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Ren, Xue
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Zhang, Xuemei
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Yang, Weifei
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Sun, Zhaoxia
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Zhang, Chunhua
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Quinet, Muriel
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Luthar, Zlata
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Germ, Mateja
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Kreft, Ivan
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Janovská, Dagmar
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Meglič, Vladimir
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Pipan, Barbara
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Georgiev, Milen I.
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Studer, Bruno
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Chapman, Mark A.
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Zhou, Meiliang
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Zhang, Kaixuan
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He, Yuqi
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Lu, Xiang
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Shi, Yaliang
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Zhao, Hui
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Li, Xiaobo
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Li, Jinlong
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Liu, Yang
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Ouyang, Yinan
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Tang, Yu
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Ren, Xue
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Zhang, Xuemei
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Yang, Weifei
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Sun, Zhaoxia
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Zhang, Chunhua
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Quinet, Muriel
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Luthar, Zlata
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Germ, Mateja
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Kreft, Ivan
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Janovská, Dagmar
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Meglič, Vladimir
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Pipan, Barbara
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Georgiev, Milen I.
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Studer, Bruno
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Chapman, Mark A.
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Zhou, Meiliang
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Zhang, Kaixuan, He, Yuqi, Lu, Xiang, Shi, Yaliang, Zhao, Hui, Li, Xiaobo, Li, Jinlong, Liu, Yang, Ouyang, Yinan, Tang, Yu, Ren, Xue, Zhang, Xuemei, Yang, Weifei, Sun, Zhaoxia, Zhang, Chunhua, Quinet, Muriel, Luthar, Zlata, Germ, Mateja, Kreft, Ivan, Janovská, Dagmar, Meglič, Vladimir, Pipan, Barbara, Georgiev, Milen I., Studer, Bruno, Chapman, Mark A. and Zhou, Meiliang (2023) Comparative and population genomics of buckwheat species reveal key determinants of flavor and fertility. Molecular Plant, 16 (9), 1427-1444. (doi:10.1016/j.molp.2023.08.013).

Record type: Article

Abstract

Common buckwheat (Fagopyrum esculentum) is an ancient crop with a world-wide distribution. Due to its excellent nutritional quality and high economic and ecological value, common buckwheat is becoming increasingly important throughout the world. The availability of a high-quality reference genome sequence and population genomic data will accelerate the breeding of common buckwheat, but the high heterozygosity due to the outcrossing nature has greatly hindered the genome assembly. Here we report the assembly of a chromosome-scale high-quality reference genome of F. esculentum var. homotropicum, a homozygous self-pollinating variant of common buckwheat. Comparative genomics revealed that two cultivated buckwheat species, common buckwheat (F. esculentum) and Tartary buckwheat (F. tataricum), underwent metabolomic divergence and ecotype differentiation. The expansion of several gene families in common buckwheat, including FhFAR genes, is associated with its wider distribution than Tartary buckwheat. Copy number variation of genes involved in the metabolism of flavonoids is associated with the difference of rutin content between common and Tartary buckwheat. Furthermore, we present a comprehensive atlas of genomic variation based on whole-genome resequencing of 572 accessions of common buckwheat. Population and evolutionary genomics reveal genetic variation associated with environmental adaptability and floral development between Chinese and non-Chinese cultivated groups. Genome-wide association analyses of multi-year agronomic traits with the content of flavonoids revealed that Fh05G014970 is a potential major regulator of flowering period, a key agronomic trait controlling the yield of outcrossing crops, and that Fh06G015130 is a crucial gene underlying flavor-associated flavonoids. Intriguingly, we found that the gene translocation and sequence variation of FhS-ELF3 contribute to the homomorphic self-compatibility of common buckwheat. Collectively, our results elucidate the genetic basis of speciation, ecological adaptation, fertility, and unique flavor of common buckwheat, and provide new resources for future genomics-assisted breeding of this economically important crop.

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Accepted/In Press date: 28 August 2023
e-pub ahead of print date: 30 August 2023
Published date: 4 September 2023
Additional Information: Funding Information: This research was supported by the National Key R&D Program of China ( 2022YFE0140800 ), the European Union Horizon 2020 project ECOBREED ( 771367 ), the Youth Innovation Program of Chinese Academy of Agricultural Sciences (No. Y2022QC02 ), Project of Sanya Yazhou Bay Science and Technology City ( SCKJ-JYRC-2022-22 ), National Natural Science Foundation of China ( 32161143005 , 31911530772 , 32111540258 ), PlantaSYST ( SGA No 739582 under FPA No. 664620 ), and the BG05M2OP001-1.003-001-C01 project, financed by the European Regional Development Fund through the “ Science and Education for Smart Growth” Operational Programme and Slovenian Research Agency , program P4-0077 “ Genetics and Modern Technologies of Crops”. Publisher Copyright: © 2023 The Author
Keywords: Fagopyrum, Fertility, Genome-Wide Association Study, Plant Breeding, flavonoids, buckwheat, natural variation, adaptation, genomics

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Local EPrints ID: 483301
URI: http://eprints.soton.ac.uk/id/eprint/483301
ISSN: 1752-9859
PURE UUID: 0efb36c9-c9fb-473b-9d88-6d94bc81908c
ORCID for Mark A. Chapman: ORCID iD orcid.org/0000-0002-7151-723X

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Date deposited: 27 Oct 2023 16:45
Last modified: 18 Mar 2024 03:24

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Contributors

Author: Kaixuan Zhang
Author: Yuqi He
Author: Xiang Lu
Author: Yaliang Shi
Author: Hui Zhao
Author: Xiaobo Li
Author: Jinlong Li
Author: Yang Liu
Author: Yinan Ouyang
Author: Yu Tang
Author: Xue Ren
Author: Xuemei Zhang
Author: Weifei Yang
Author: Zhaoxia Sun
Author: Chunhua Zhang
Author: Muriel Quinet
Author: Zlata Luthar
Author: Mateja Germ
Author: Ivan Kreft
Author: Dagmar Janovská
Author: Vladimir Meglič
Author: Barbara Pipan
Author: Milen I. Georgiev
Author: Bruno Studer
Author: Mark A. Chapman ORCID iD
Author: Meiliang Zhou

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